Signaling mechanisms for activation of extracytoplasmic function (ECF) sigma factors

Brooks, Benjamin E.; Buchanan, Susan K.

doi:10.1016/j.bbamem.2007.06.005

Cited by 86 publications

(92 citation statements)

References 129 publications

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“…The necessary means for bacterial adaptation processes critically rely on sensing and quickly responding to the specific extracellular conditions encountered. One common way to achieve rapid activation of genes in response to fluctuating environmental conditions is the use of extracytoplasmic function (ECF) sigma () factors that are especially abundant in P. aeruginosa (1,2). ECF factors serve as important regulators, and they are increasingly recognized as factors regulating expression of virulence genes and virulence-associated genes (3)(4)(5).…”

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confidence: 99%

Identification of the Alternative Sigma Factor SigX Regulon and Its Implications for Pseudomonas aeruginosa Pathogenicity

Blanka

Schulz

Eckweiler

et al. 2013

Journal of Bacteriology

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e Pseudomonas aeruginosa is distinguished by its broad metabolic diversity and its remarkable capability for adaptation, which relies on a large collection of transcriptional regulators and alternative sigma () factors. The largest group of alternative factors is that of the extracytoplasmic function (ECF) factors, which control key transduction pathways for maintenance of envelope homeostasis in response to external stress and cell growth. In addition, there are specific roles of alternative factors in regulating the expression of virulence and virulence-associated genes. Here, we analyzed a deletion mutant of the ECF factor SigX and applied mRNA profiling to define the SigX-dependent regulon in P. aeruginosa in response to low-osmolarity-medium conditions. Furthermore, the combination of transcriptional data with chromatin immunoprecipitation (ChIP) followed by high-throughput sequencing (ChIP-seq) led to the identification of the DNA binding motif of SigX. Genome-wide mapping of SigX-binding regions revealed enrichment of downstream genes involved in fatty acid biosynthesis, type III secretion, swarming and cyclic di-GMP (c-di-GMP) signaling. In accordance, a sigX deletion mutant exhibited altered fatty acid composition of the cell membrane, reduced cytotoxicity, impaired swarming activity, elevated c-di-GMP levels, and increased biofilm formation. In conclusion, a combination of ChIP-seq with transcriptional profiling and bioinformatic approaches to define consensus DNA binding sequences proved to be effective for the elucidation of the regulon of the alternative factor SigX, revealing its role in complex virulence-associated phenotypes in P. aeruginosa. Pseudomonas aeruginosa is an opportunistic bacterial pathogen that can be distinguished by its exceptional high capability to adapt and survive in various and challenging habitats and hosts, including animals, plants, and the human host. The necessary means for bacterial adaptation processes critically rely on sensing and quickly responding to the specific extracellular conditions encountered. One common way to achieve rapid activation of genes in response to fluctuating environmental conditions is the use of extracytoplasmic function (ECF) sigma () factors that are especially abundant in P. aeruginosa (1, 2). ECF factors serve as important regulators, and they are increasingly recognized as factors regulating expression of virulence genes and virulence-associated genes (3-5). The activity of most of the ECF factors are modulated by inner membrane sensor proteins that act as antisigma factors. An off-switch of the anti-sigma factor in response to specific environmental changes thereby presumably leads to the release of the cognate factor and thus allows recruitment of the RNA polymerase to initiate expression of the specific factordependent gene regulon (6). So far, cell envelope stress, iron limitation, and oxidative stress have been demonstrated to play a pivotal role during host infection and were described to activate ECF factors (7,8). In addition to th...

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confidence: 99%

Identification of the Alternative Sigma Factor SigX Regulon and Its Implications for Pseudomonas aeruginosa Pathogenicity

Blanka

Schulz

Eckweiler

et al. 2013

Journal of Bacteriology

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“…In general, each factor is cotranscribed with an adjacent gene encoding an antifactor, which is usually a membrane protein that sequesters its cognate factor to the cytoplasmic membrane (66). In response to an inducing signal, the anti-factor is inactivated, often by proteolytic degradation (11,31). The released factor then binds core RNA polymerase (RNAP) and directs the activation of specific promoter sites.…”

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Bacillus subtilis σ ^V Confers Lysozyme Resistance by Activation of Two Cell Wall Modification Pathways, Peptidoglycan O-Acetylation and d -Alanylation of Teichoic Acids

2011

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The seven extracytoplasmic function (ECF) sigma () factors of Bacillus subtilis are broadly implicated in resistance to antibiotics and other cell envelope stressors mediated, in part, by regulation of cell envelope synthesis and modification enzymes. We here define the regulon of V as including at least 20 operons, many of which are also regulated by M , X , or W . The V regulon is strongly and specifically induced by lysozyme, and this induction is key to the intrinsic resistance of B. subtilis to lysozyme. Strains with null mutations in either sigV or all seven ECF factor genes (⌬7ECF) have essentially equal increases in sensitivity to lysozyme. Induction of V in the ⌬7ECF background restores lysozyme resistance, whereas induction of M , X , or W does not. Lysozyme resistance results from the ability of V to activate the transcription of two operons: the autoregulated sigV-rsiV-oatA-yrhK operon and dltABCDE. Genetic analyses reveal that oatA and dlt are largely redundant with respect to lysozyme sensitivity: single mutants are not affected in lysozyme sensitivity, whereas an oatA dltA double mutant is as sensitive as a sigV null strain. Moreover, the sigV oatA dltA triple mutant is no more sensitive than the oatA dltA double mutant, indicating that there are no other V -dependent genes necessary for lysozyme resistance. Thus, we suggest that V confers lysozyme resistance by the activation of two cell wall modification pathways: O-acetylation of peptidoglycan catalyzed by OatA and D-alanylation of teichoic acids by DltABCDE.

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“…ECF sigma factors typically sense and respond to changes in the extracellular environment, including oxidative stress, misfolded proteins, and changes in temperature, pressure, or nutrient concentration (26,27). The ECF sigma factor family is the largest and most divergent of the bacterial sigma factor families (25).…”

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The Bartonella quintana Extracytoplasmic Function Sigma Factor RpoE Has a Role in Bacterial Adaptation to the Arthropod Vector Environment

Abromaitis

Koehler

2013

J Bacteriol

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Bartonella quintana is a vector-borne bacterial pathogen that causes fatal disease in humans. During the infectious cycle, B. quintana transitions from the hemin-restricted human bloodstream to the hemin-rich body louse vector. Because extracytoplasmic function (ECF) sigma factors often regulate adaptation to environmental changes, we hypothesized that a previously unstudied B. quintana ECF sigma factor, RpoE, is involved in the transition from the human host to the body louse vector. The genomic context of B. quintana rpoE identified it as a member of the ECF15 family of sigma factors found only in alphaproteobacteria. ECF15 sigma factors are believed to be the master regulators of the general stress response in alphaproteobacteria. In this study, we examined the B. quintana RpoE response to two stressors that are encountered in the body louse vector environment, a decreased temperature and an increased hemin concentration. We determined that the expression of rpoE is significantly upregulated at the body louse (28°C) versus the human host (37°C) temperature. rpoE expression also was upregulated when B. quintana was exposed to high hemin concentrations. In vitro and in vivo analyses demonstrated that RpoE function is regulated by a mechanism involving the anti-sigma factor NepR and the response regulator PhyR. The ⌬rpoE ⌬nepR mutant strain of B. quintana established that RpoE-mediated transcription is important in mediating the tolerance of B. quintana to high hemin concentrations. We present the first analysis of an ECF15 sigma factor in a vector-borne human pathogen and conclude that RpoE has a role in the adaptation of B. quintana to the hemin-rich arthropod vector environment.

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Signaling mechanisms for activation of extracytoplasmic function (ECF) sigma factors

Cited by 86 publications

References 129 publications

Identification of the Alternative Sigma Factor SigX Regulon and Its Implications for Pseudomonas aeruginosa Pathogenicity

Identification of the Alternative Sigma Factor SigX Regulon and Its Implications for Pseudomonas aeruginosa Pathogenicity

Bacillus subtilis σ ^V Confers Lysozyme Resistance by Activation of Two Cell Wall Modification Pathways, Peptidoglycan O-Acetylation and d -Alanylation of Teichoic Acids

The Bartonella quintana Extracytoplasmic Function Sigma Factor RpoE Has a Role in Bacterial Adaptation to the Arthropod Vector Environment

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Signaling mechanisms for activation of extracytoplasmic function (ECF) sigma factors

Cited by 86 publications

References 129 publications

Identification of the Alternative Sigma Factor SigX Regulon and Its Implications for Pseudomonas aeruginosa Pathogenicity

Identification of the Alternative Sigma Factor SigX Regulon and Its Implications for Pseudomonas aeruginosa Pathogenicity

Bacillus subtilis σ V Confers Lysozyme Resistance by Activation of Two Cell Wall Modification Pathways, Peptidoglycan O-Acetylation and d -Alanylation of Teichoic Acids

The Bartonella quintana Extracytoplasmic Function Sigma Factor RpoE Has a Role in Bacterial Adaptation to the Arthropod Vector Environment

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Bacillus subtilis σ ^V Confers Lysozyme Resistance by Activation of Two Cell Wall Modification Pathways, Peptidoglycan O-Acetylation and d -Alanylation of Teichoic Acids